Aim

For tens of millions of years, herbivorous megafauna were abundant across the globe, fulfilling important ecological roles including seed dispersal. Megafruits are very large fruits that are dispersed most effectively by megafauna. However, megafruits also occur in ecosystems where megafauna are extinct or were never present, emphasizing our incomplete understanding of megafauna-megafruit relationships. Here we use the complex biogeography of tropical Asia to investigate how megafruit diversity and traits are associated with the diversity of megafauna, smaller animals, and abiotic factors.

Location

Tropical Asia, from the Indian subcontinent in the west to tropical China in the north to the Maluku archipelago (Indonesia) in the east.

Time period

Late Pleistocene to the present day.

Major taxa studied

Megafauna (body weight >500 kg) that consume fruits, including stegodons, elephants, rhinoceroses, giant tapirs, and large bovids. Fleshy-fruited plant species across the region with a fruit width >40 mm (i.e., megafruits).

Methods

We compiled a list of all megafruits along with selected plant, fruit, and seed traits in 16 subregions across tropical Asia. We explored biogeographic patterns in megafruit diversity and traits in relation to the diversities of past and present megafauna, large- and medium-sized animals and abiotic factors (mean temperature, mean precipitation, precipitation seasonality, insularity).

Results

We identified 496 megafruits in tropical Asia. Megafruit diversity was highest in subregions with high megafaunal diversity, particularly extant species. Megafruit traits were influenced most strongly by abiotic factors (mainly temperature and land area), and weakly by megafauna and smaller dispersers.

Main conclusions

Our results are consistent with megafauna maintaining or responding to megafruit diversity, but variation in megafruit traits is primarily associated with abiotic factors. Given the massive megafaunal losses in tropical Asia since the Late Pleistocene, it is important to identify fruit traits that can increase megafauna-dependence and thus vulnerability to these losses.

Our study area encompassed the Indian subcontinent, north to tropical China and east to the Maluku Islands of Indonesia. We recorded megafruits, megafaunal animals, and other potential consumers of megafruits in these subregions. We use the term “diversity” to refer to the number of species for each of these. For each of these variables we gathered species lists from regional floras and published literature.

We used personal experience and floras from across the region to identify megafruits. Our searches were exhaustive, but we could have missed a few species for which fruit trait information was not available. The criteria for inclusion were fruit width ≥40 mm (Guimarães et al., 2008) and having an edible fruit-part other than the seed. For genera with several species of megafruits, where some lacked size information, we used additional resources (internet searches, unpublished data) to obtain fruit descriptions. Sixty-nine of the 496 species of megafruits did not have fruit width information available but were included because the genera had many other megafruit species. Half of these species (N = 30) were in Rafflesia, whose dispersers are almost completely unknown (Hidayati and Walck, 2016). The presence or absence of all the megafruit species in our list was recorded for each of the 16 biogeographic subregions. 

The following details were recorded for the fruit when available: IUCN status, habitat type, growth form (climber, tree, palm, shrub, herb), tree height, fruit-type (berry, drupe, syncarp, syconium, capsule, pod, follicles) and fruit colour. Fruit colour was simplified to the main colour displayed (see below) and then condensed into two broad groups that reflected consumption by terrestrial, dichromatic mammals (Yokoyama et al., 2005) and megafauna (Bunney et al., 2019). Brown, green, yellow, or orange fruits were grouped as being primarily targeted towards these mammals (“megafauna-coloured”), either because the fruit had not invested resources in colours that are not perceived as distinct by dichromats, or because they had invested in odour instead (Valenta et al., 2018), or possibly because these dull colours allowed fruits to escape predation on the forest floor. The other colour grouping – red, black, purple, pink, white, and blue – were fruits that had invested in colours often associated with tetrachromatic birds and, possibly, also perceived by trichromatic primates. The measured characteristics were fruit length (longest axis) and width (second longest axis), seed length and width, and seed number per fruit. Data were collected from published floras from different subregions, journal publications, and other on-line sources (only when published information was unavailable). The references used are recorded in the database.

The nomenclatures and distributions of the 495 species in our database were checked in Plants of the World Online database (POWO). Synonyms were removed and distributions changed to follow POWO in 105 of the 157 discrepancies that we observed. For the other 52 species, we followed recent publications and regional floras that were available on-line. 

Literature cited

Bunney, K., Robertson, M. & Bond, W. (2019). The historical distribution of megaherbivores does not determine the distribution of megafaunal fruit in southern Africa. Biological Journal of the Linnean Society 128, 1039–1051.

Guimarães, P. R., Galetti, M. & Jordano, P. (2008). Seed Dispersal Anachronisms: Rethinking the Fruits Extinct Megafauna Ate. PLoS ONE 3, e1745 (2008).

Hidayati, S. N. & Walck, J. L. (2016). A review of the biology of Rafflesia: what do we know and what’s next? Bulletin Kebun Raya 9, 67–78.

POWO. (2020). Plants of the World Online | Kew Science. Plants of the World Online http://www.plantsoftheworldonline.org/.

Valenta, K., Kalbitzer, U., Razafimandimby, D., Omeja, P., Ayasse, M., Chapman, C. A., Nevo, O. (2018). The evolution of fruit colour: phylogeny, abiotic factors and the role of mutualists. Scientific Reports 8, 14302.

Yokoyama, S., Takenaka, N., Agnew, D. W. & Shoshani, J. (2005). Elephants and Human Color-Blind Deuteranopes Have Identical Sets of Visual Pigments. Genetics 170, 335–344.

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